Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012

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1 Surveillnce nd outrek reports Lrge multistte outrek of norovirus gstroenteritis ssocited with frozen strwerries, Germny, 212 H Bernrd 1,2, M Fer (ferm@rki.de) 1,2, H Wilking 1, S Hller 1,3,4, M Höhle 1, A Schielke 1, T Ducomle 1,4,5, C Siffczyk 6, S S Merecks 7, G Fricke 8, O Hmoud 1, K Strk 1, D Werer 1, on ehlf of the Outrek Investigtion Tem 9 1. Roert Koch Institute, Berlin, Germny 2. These uthors contriuted eqully 3. Postgrdute Trining for Applied Epidemiology, Berlin, Germny 4. Europen Progrmme for Intervention Epidemiology, Stockholm, Sweden 5. Europen Centre for Disese Prevention nd Control, Stockholm, Sweden 6. Stte Helth Authority Brndenurg, Zossen, Germny 7. Stte Helth Authority Sxony, Chemnitz, Germny 8. Federl Office of Consumer Protection nd Food Sfety, Berlin, Germny 9. The tem memers re listed t the end of the mnuscript Cittion style for this rticle: Bernrd H, Fer M, Wilking H, Hller S, Höhle M, Schielke A, Ducomle T, Siffczyk C, Merecks SS, Fricke G, Hmoud O, Strk K, Werer D, on ehlf of the Outrek Investigtion Tem. Lrge multistte outrek of norovirus gstroenteritis ssocited with frozen strwerries, Germny, 212. Euro Surveill. 214;19(8):pii=2719. Aville online: Article sumitted on 24 Jnury 213 / pulished on 27 Ferury 214 From 2 Septemer through 5 Octoer 212, the lrgest recorded food-orne outrek in Germny occurred. Norovirus ws identified s the custive gent. We conducted four nlyticl epidemiologicl studies, two cse control studies nd two surveys (in totl 15 cses) in secondry schools in three different federl sttes. Overll, 39 institutions in five federl sttes reported nerly 11, cses of gstroenteritis. They were predominntly schools nd childcre fcilities nd were supplied lmost exclusively y one lrge ctering compny. The nlyticl epidemiologicl studies consistently identified dishes contining strwerries s the most likely vehicle, with estimted odds rtios rnging from 2.6 to The dishes hd een prepred in different regionl kitchens of the ctering compny nd were served in the schools two dys efore the peks of the respective outreks. All ffected institutions hd received strwerries of one lot, imported frozen from Chin. The outrek vehicle ws identified within week, which led to timely recll nd prevented more thn hlf of the lot from reching the consumer. This outrek exemplifies the risk of lrge outreks in the er of glol food trde. It underlines the importnce of timely surveillnce nd epidemiologicl outrek investigtions for food sfety. Introduction Infection with norovirus is the most common cuse of cute infectious gstroenteritis in Europen countries [1,2], usully mnifesting with self-limiting symptoms of vomiting nd dirrhoe, with sudden onset nd short durtion [3]. Lrge protrcted outreks of norovirus gstroenteritis re often recognised in institutions such s hospitls nd homes for the elderly [4], with person-to-person trnsmission predominting. Food-orne norovirus outreks re common, ut still under-recognised [5,6]. In Germny, outreks of cute infectious gstroenteritis re notifile to the locl pulic helth deprtments ccording to the Protection Aginst Infection Act of 21. The helth deprtments conduct epidemiologicl investigtions nd tke control mesures. They lso trnsmit outrek informtion electroniclly to the pulic helth uthority of the respective federl stte nd, susequently, to the Roert Koch Institute (RKI) on the ntionl level [7]. On request of the stte helth uthorities, the RKI ssists in outrek investigtions, including nlyticl epidemiologicl studies. On mid-dy of 27 Septemer 212, the pulic helth uthority of the federl stte of Brndenurg informed the RKI out severl outreks of gstroenteritis in schools nd childcre fcilities in Brndenurg mssing to t lest 5 cses. Dirrhoe or vomiting in ffected individuls hd strted on the evening efore. All ffected institutions offered lunch provided y Cterer X, compny operting cross Germny, nd food-orne outrek ws suspected. According to the pulic helth deprtment of one of the ffected counties, Cterer X ws lredy wre of gstroenteritis cses in four other Germn federl sttes (Berlin, Sxony-Anhlt, Sxony nd Thuringi). The RKI informed the two ntionl food sfety uthorities, the Federl Institute for Risk Assessment (BfR) nd the Federl Office of Consumer Protection nd Food Sfety (BVL), nd the pulic helth uthorities of the other 15 federl sttes out the sitution nd requested informtion on similr outreks. By the evening of the sme dy, the RKI hd knowledge of more thn 4, cses relting to outreks in schools nd childcre 1

2 fcilities supplied y Cterer X in four neighouring federl sttes in the est of Germny. This report focusses on the epidemiologicl investigtions to identify the outrek vehicle nd to prevent further cses. Detils of the lortory investigtions re presented elsewhere [8]. Methods Descriptive nlysis In dily teleconferences, the pulic helth uthorities of the ffected federl sttes nd the RKI exchnged informtion on the numer of ffected institutions (including ggregted cse numers) nd on lortory results from humn smples tken in the context of the outrek. For the descriptive nlysis, we defined cse s person with dirrhoe or vomiting from 19 Septemer through 7 Octoer 212, who did not test positive for ny pthogen other thn norovirus nd who ttended n ffected institution. An institution ws considered to e ffected if it offered mels y ny externl cterer nd if t lest 1 cses hd occurred in tht institution (or, in smll institutions, if 1% of persons were cses). We did not restrict ffected institutions to those supplied y Cterer X to remin sensitive to the potentil involvement of other cterers in this outrek. Anlyticl studies On the individul level we conducted two cse control studies (CCS) nd two surveys in ffected secondry schools in three federl sttes. For the CCS, we interviewed pupils directly t their schools, for the surveys, we-sed (Survey 1) nd n emil (Survey 2) questionnire were used. Exposure histories were recorded for menu items offered in these schools for lunch (s listed on weekly menu plns) nd other food items ville in the school, e.g. in the cfeteri. The cnteens of ll four schools hd een supplied y different regionl kitchens of Cterer X. The custive gent ws unknown t the strt of ll four studies, ut ws suspected to e norovirus or cteril toxins, sed on reported symptoms nd the sudden nd lmost simultneous occurrence of disese within the institutions. Thus, the relevnt period of exposure ws considered to e the three dys efore the strt of the outreks in these institutions (the dtes were not identicl t the four study sites). In ll four studies, we investigted whether eting t the school cnteen ws ssocited with illness. We restricted the clcultion of food-specific ssocitions to individuls who reported hving hd lunch t the school cnteen on ny of the dys of the exposure period. Pupils who reported gstroenteric illness in the fmily in the week efore the outrek period were excluded from the nlysis ecuse they could hve een secondry cses of illness in their household. We compred cses nd controls regrding their food exposures, clculted odds rtios (ORs) nd 95% confidence intervls (CI), nd ssessed sttisticl significnce using Fisher s exct or other pproprite tests. If severl food items were ssocited with disese in univrile nlyses with n OR>1, p vlue <.2 nd n exposure reported y t lest 25% of cses, multivrile logistic regression nlysis (exct method for the surveys) ws performed with mnul forwrd selection of vriles (cut-off: p<.2). Sttisticl nlyses were conducted in R [9] for the CCS nd Stt [1] for the surveys. Cse control study 1 CCS1 ws conducted on 1 nd 2 Octoer in School A in city in Sxony. The school hd experienced sudden surge of gstroenteritis cses during clendr week 39 (24 3 Septemer) with pek on Wednesdy, 26 Septemer, nd hd een closed on 28 Septemer due to the outrek. We restricted the study to pupils from grdes 5 to 7 (1 13 yer-olds) ecuse these ge groups were predominntly ffected in this school. We defined cse s pupil with onset of vomiting or dirrhoe from 24 to 3 Septemer (outrek period for CCS1). Of the pproximtely 7 cses, we selected two thirds for the study using systemtic rndom smpling. Eligile controls were ll pupils from three school clsses who did not report vomiting or dirrhoe during the outrek period. The clsses were ritrrily chosen y the deputy hed of the school. Assuming n exposure prevlence of 7% mong cses, cse-to-control rtio of 1 would hve llowed us to detect n OR of 4 with power of 86% t significnce level of 5%. We collected informtion on the prticipnts ge nd sex, symptoms, dte of symptom onset nd on food exposures t the school s cnteen during clendr week 39, s indicted y the cnteen s menu pln, which listed four mel choices dily. For dt entry nd immedite univrile nlysis on site, we used the Linelist tool, spredsheet file developed t the RKI, to ssist in the epidemiologic investigtion of locl outreks [11]. On 2 Octoer, we conducted su-study restricting the study popultion to those who hd reported eting t the school cnteen on Mondy 24 Septemer. Cses with symptom onset fter 28 Septemer were excluded from the nlysis. In this su-study, prticipnts were explicitly sked for the consumption of strwerry compote ecuse it hd not only een prt of one min mel ut lso een offered s dessert with two of the other three mel choices. The informtion ws collected in n ggregte fshion during congregtion of cses nd controls in the school uditorium, y sending ech pupil to one of four corners depending on the pupils outcome nd exposure sttus ( live 2x2 tle). The children were first split into two groups sed on presence of symptoms, nd these groups were divided further sed on their recollection of hving eten strwerries. Pupils were explicitly told not 2

3 to wlk with their friends, ut ccording to their recollection of symptoms nd food consumption. Cse control study 2 CCS2 ws conducted on 4 Octoer in School B in the stte of Thuringi. The school hd not een closed in response to the outrek. The im of the study ws to investigte whether the results of CCS1 were reproducile in different geogrphicl region. The methodology ws identicl to CCS1 with the following exceptions: Pupils from grde 8 (14 yers-old) were dditionlly included, the outrek period ws from 24 through 27 Septemer, nd eligile controls cme from five ritrrily chosen clsses. Becuse strwerry compote ws offered s dessert with severl mel choices, even on the sme dy, we sked for this food item in n dditionl question. Survey 1 (we-sed questionnire) This study ws conducted t School C locted in Sxony using n online questionnire. The school hd experienced sudden surge of gstroenteritis cses during the lst two weeks of Septemer nd, in response to the outrek, hd een closed on Fridy 28 Septemer. Lunches consisted of min component (e.g. chicken wings), pre-ordered y the pupils nd dispensed y cnteen stff, nd side dishes, slds nd desserts for self-service uffet crt. Study prticipnts were recruited through letter, distriuted y techers nd ddressed to the prents of ll pupils of grdes 5 to 8 (n=451) present t the school on 5 Octoer. It informed out the ims of the study nd invited prticiption in n online survey. The questionnire ws ccessile (pssword-protected) from 5 Octoer through 8 Octoer. It contined questions on demogrphy (ge, sex, grde), potentil disese history (symptoms, time course) nd food exposure history from 2 through 27 Septemer (choice of three min components nd round 1 sides nd desserts dily). We defined cse s pupil with onset of vomiting or dirrhoe from 2 through 29 Septemer. Cses with n onset dte 2 23, nd Septemer were defined s first-, second- nd thirdwve cses, respectively. Survey 2 (emil questionnire) This study ws conducted t School D in Berlin. On 5 Octoer, 38 cses of gstroenteritis hd een notified to the locl helth deprtment y the hed of the school. Becuse school holidys hd just egun t the strt of the study, fce-to-fce interviews were not fesile. We therefore developed questionnire covering, in ddition to demogrphic nd symptom informtion, mels served etween 24 nd 28 Septemer (choice of four dishes dily plus sld uffet). This questionnire ws emiled to the prents of ll pupils under the ge of 18 yers (pproximtely n=9). Questionnires could e returned to the RKI vi electronic or regulr mil etween 1 nd 5 Octoer. Cses were defined s pupils with onset of dirrhoe nd/or vomiting from 24 through 28 Septemer. Food trce-ck investigtions The Germn Tsk Force on Food nd Feed sfety, consisting of food sfety uthorities of ffected sttes nd t the ntionl level, convened on 29 Septemer. The tsk force coordinted food sfety investigtions, which lso included epidemiologicl product trcing investigtions. Results Descriptive nlysis A totl of 39 institutions in five federl sttes in Est Germny were reported s ffected during the outrek period. The erliest outrek in n institution strted on 2 Septemer, the ltest on 5 Octoer, nd most strted etween 25 nd 28 Septemer with pek on 27 Septemer (n=18 institutions, 28%) (Figure 1). A medin of 21 children were ffected per institution (inter-qurtile rnge (IQR): 12 37). The mjority of ffected institutions were schools (244/39, 63%) nd childcre fcilities (14/39, 36%), three were fcilities for disility cre, two were homes for the elderly nd one ws rehilittion clinic. A totl of 1,95 persons, mostly children nd teengers ut lso stff memers, were reported ill in the ffected institutions. The medin proportion of cses mong regulr ttendees ws 14% (IQR: 1 22) cross ll ffected institutions, nd 18% (IQR: 12 27) in childcre fcilities. At lest 38 (.3%) people required hospitlistion; the mjority of illnesses were of short durtion nd self-limiting. Figure 2 shows the incidence of illnesses mong persons under the ge of 18 yers y district. The federl sttes of Sxony, Brndenurg nd Berlin were predominntly ffected, which lso reflects the distriution of ffected institutions (n=13, 129 nd 88, respectively). Figure 1 Numer of ffected institutions y dte of onset of first cse in the respective institution, multistte outrek of norovirus gstroenteritis, Germny, 212 (n=39 ) Affected institutions We Th Fr S Su Mo Tu We Th Fr S Su Mo Tu We Th Fr S Su Septemer 212 Octoer 212 Dte of symptom onset of first cse Dte of onset of first cse ws ville for 39 institutions. 3

4 As of 8 Octoer 212, 555 humn specimens (339 from ill persons, nd convenience smple of 216 stff memers of Cterer X with unknown disese sttus) were reported y the helth uthorities of four of the five ffected federl sttes. Of those, 32% were positive for norovirus (4% of ill persons, 2% of stff memers). No other virl or cteril pthogens or cteril toxins were reported from the respective helth deprtments in connection with the outrek. Anlyticl studies All four nlyticl studies, comprising 15 cses nd 274 controls, identified dishes contining strwerries s vehicles of infection (either strwerry compote or strwerry fruit qurk) (Tle). Cse control study 1 We included 43 cses nd 54 controls (medin ge for ech: 11 yers), three potentil secondry household cses were excluded. Symptom onset ws from 24 through 3 Septemer, with steep increse nd pek of the epidemic curve on Wednesdy 26 Septemer (n=16 cses) suggesting point source (Figure 3A). Most cses, nd higher proportion of cses thn controls, hd eten t the school s cnteen on Mondy 24 nd Tuesdy 25 Septemer (see Tle), ut not on the following two dys (when sustntil proportion of cses were lredy sick). The only dish offered on one of these two dys tht ws positively ssocited Figure 2 Cses per 1, popultion under the ge of 18 yers y districts, nd loctions of nlyticl study sites, multistte outrek of norovirus gstroenteritis, Germny, 212 (n=1,95) Brndenurg Sxony-Anhlt D Incidence < ,376 >1,376 Study sites A: Cse control study 1 B: Cse control study 2 C: Survey 1 D: Survey 2 Thuringi Sxony B C A km 4

5 Tle Results of univrile nd multivrile risk fctor nlyses, multistte outrek of norovirus gstroenteritis, Germny, 212 (n=424) School lunch exposure Cses Controls Univrile nlysis Multivrile nlysis Totl Exposed (%) Totl Exposed (%) OR 95% CI p vlue OR 95% CI p vlue Cse control study 1 Mon 24 Sep (84) (76) Semolin pudding nd strwerry compote (72) 4 2 (5) Any strwerry contining dish (89) 4 27 (68) Strwerry compote c (76) 4 11 (28) <.1 Not performed Tue 25 Sep (81) (7) Wed 26 Sep (56) (72) Thu 27 Sep (4) (7) <.1 Cse control study 2 Mon 24 Sep (95) 73 4 (55) <.1 Semolin pudding nd strwerry compote 37 3 (81) 4 17 (43) <.1 Strwerry compote (86) 4 11 (28) < <.1 Tue 25 Sep (85) (58) Pst Bolognese (82) (6) Wed 26 Sep 39 3 (8) 73 3 (41) <.1 Thu 27 Sep 39 9 (23) (37) Survey 1 First wve Thu 2 Sep: Strwerry fruit qurk (88) 6 15 (25) < <.1 Thu 2 Sep: Fresh plums 2 7 (35) 53 1 (19) Second wve Mon 24 Sep: Strwerry compote (75) 27 3 (11) < <.1 Tue 25 Sep: Pes nd crrots 15 9 (6) 27 2 (7) < <.1 Tue 25 Sep: Red cge 15 7 (47) 3 5 (17) Tue 25 Sep: Suce (78) (5) Mon 24 Sep: Semolin pudding (72) (53) Tue 25 Sep: Boiled pottoes 14 8 (57) 28 1 (36) Third wve Wed 26 Sep: Strwerry qurk dessert 7 5 (71) 25 1 (4) , < , <.1 Mon 24 Sep: Fruit yoghurt 7 5 (71) 26 4 (15) <.1 Tue 25 Sep: Plin yoghurt 8 4 (5) 24 4 (17) Survey 2 Any school lunch Sep (1) (35) <.1 Wed 26 Sep: Semolin pudding nd strwerry compote 14 1 (71) 25 3 (12) <.1 Not performed Wed 26 Sep: Strwerry compote (with ny dish) (92) 21 5 (24) ,65.8 <.1 CI: confidence intervl; OR: odds rtio. Only exposures positively ssocited with disese occurrence with p<.2 nd explining t lest 25% of cses re shown. Not considered for multivrile nlysis. Not prt of the finl multivrile model, i.e. p.2. c Results from su-study ( live 2x2 tle ). 5

6 with illness with p vlue <.1, ws semolin pudding, which hd een served on Mondy with choice of cherries, sugr nd cinnmon, or cold strwerry compote (Tle). Of the 36 cses, 26 reported to hve chosen the semolin pudding. However, on tht dy strwerry compote hd een offered with three of the four mel choices. We therefore compred cses nd controls regrding the choice of ny mel contining strwerry compote. Cses hd chosen significntly (p<.5) more often strwerry compote-contining dish thn controls. In the su-study including those who hd eten t the cnteen on Mondy 24 Septemer, 28 of 37 cses ut only 11 of 4 controls reported to hve eten strwerry compote (OR=8.2; 95% CI: ; p<.1). Hving identified dish served on Mondy 24 Septemer s the likely vehicle of infection, we estimted medin incution period of two dys (IQR: 2 6 dys; onset dt only ville y full dys). Figure 3 Time course of the norovirus outrek: numer of cses included in the four nlyticl studies, y dte of symptom onset, Germny, 212 (n=148) School A, Sxony (n=43) School B, Thuringi (n=39) Cse control study 2 We included 39 cses nd 73 controls in the nlysis (medin ge: 11 nd 12 yers, respectively), excluding gin three potentil household secondry cses. The epidemic curve showed n even steeper increse in cse numers with 36 of 39 of cses with symptom onset on Tuesdy 25 (n=17) or Wednesdy 26 (n=19) Septemer (Figure 3B). Most cses, nd higher proportion of cses thn controls, hd eten t the school s cnteen on Mondy 24 nd Tuesdy 25 Septemer (see Tle), ut not on the following two dys (when sustntil proportion of cses were lredy sick). On oth dys, the consumption of one dish ws significntly ssocited with illness: semolin pudding with strwerry compote, sugr nd cinnmon on Mondy, nd pst with Bolognese suce on Tuesdy (Tle). Agin, the strwerry compote hd een offered with two of the four dishes on Mondy, nd the ssocition etween consumption nd illness ws even stronger when nlysing compote s seprte vrile. In multivrile nlyses including the exposure vriles strwerry compote on Mondy nd pst on Tuesdy, only the consumption of strwerry compote remined significntly ssocited with illness (OR=16.87; 95% CI: ; p<.1). Survey 1 (we-sed questionnire) We included 54 cses nd 75 controls (medin ge of ech: 12 yers) in the nlysis (prticiption rte: 29%). The epidemic curve showed three peks of dtes of symptom onset (Figure 3C). Overll, the proportion of persons hving hd lunch t the school cnteen from 2 through 27 Septemer ws significntly higher in cses thn in controls (98% vs 76%, OR=16.7; 95% CI: ; p<.1). Numer of cses School C, Sxony (n=53) School D, Berlin (n=13) In univrile nlyses (Tle) we found n ssocition etween eing cse in the first wve nd the consumption of strwerry qurk nd fresh plums oth served on 2 Septemer. In the multivrile nlysis, only the former remined sttisticlly significnt (OR=27.13; 95% CI: ; p<.1). For the cses in the second wve, we found significnt ssocition with hving eten t the school cnteen on 24 Septemer (multivrile nlysis: OR=11.1; 95% CI: ; p<.5). Of the 35 items served on tht nd the following dy, six were ssocited with disese nd included in the multivrile nlysis, in which strwerry compote (OR=33.8; 95% CI: 3.41 ; p<.1) nd crrots nd pes (OR=23.66; 95% CI: 2.22 ; p<.1) remined significnt. 16 Sep 23 Sep 3 Sep 7 Oct Dte of symptom onset, 212 The columns for School C re filled with different colours for the three wves of disese (see cse definition). For cses in the third wve, the univrile nlysis showed three different food items to e ssocited with occurrence of disese. In the multivrile nlysis only strwerry qurk remined sttisticlly significnt (OR=45.42; 95% CI: ,944.92; p<.1). 6

7 Survey 2 (emil questionnire) We received 86 completed questionnires (response 1%). 14 prticipnts were clssified s cses, 72 s controls. Medin ge of cses nd controls ws 12 yers (rnge: 9 16 nd 9 17, respectively). Onset times peked on the fternoon of 27 Septemer nd the following morning (Figure 3D). The proportion of persons hving eten t the school s cnteen from 24 through 28 Septemer ws significntly higher in cses thn in controls. Of ll dishes on offer during tht period, only semolin pudding with strwerry compote resulted in sttisticlly significnt positive ssocition with disese in the univrile nlysis (Tle). Strwerry compote ws lso offered s dessert longside Chin vegetles, ut only one pupil reported to hve chosen this dish. The strongest ssocition ws found when sking specificlly for the consumption of strwerry compote (independent of min course). The medin incution period, clculted from the most likely time of exposure to strwerries (13: on 26 Septemer) nd the individul times of symptom onset, ws 35 hours (rnge: 12 4 hours). Food trce-ck investigtions Frozen strwerries hd een used in regionl kitchens of Cterer X. They were prt of lot of 22 tonnes imported y Compny Y in Sxony from compny in Chin, pckged in 2,21 oxes of 1 kg ech. Of the institutions with ville informtion, 98% (368/377) were supplied y regionl kitchens of Cterer X, the reminder were supplied y two smller ctering compnies. All three cterers were supplied y the sme compny (Compny Y). All ffected institutions hd received products contining the implicted frozen strwerries. Strting on 5 Octoer, the dte of joint press relese y RKI, BfR nd BVL, Compny Y egn withdrwing the lot of frozen strwerries from their customers (the compny hd lredy stopped further delivery of the strwerries efore tht dte). Overll, delivery stop nd recll ensured tht t lest 1,136 oxes (more thn 11 tons) of strwerries from the incriminted lot did not rech the consumer. The remining 1,65 oxes (c 1.7 tons) hd either lredy een used or were destroyed under the supervision of the locl food sfety uthorities fter the recll. On Oct 8, Sxony s Stte Helth Lortory detected norovirus in smple otined from n unopened ox of the incriminted lot of frozen strwerries [12]. Discussion We report here the lrgest recorded food-orne outrek in Germny. It ffected severl hundreds of institutions supplied lmost exclusively y one lrge cterer nd ws ssocited with strwerries imported frozen in lrge lot from Chin. Norovirus ws identified s the custive gent. Although the individul clinicl courses of disese were mild, the overll disese urden ws considerle. The high numer of cses cused sustntil distress nd impirment of the dily routine in ffected institutions nd fmilies, considerle concerns out food sfety in cnteens for children, nd ntionwide medi interest. The epidemiologicl studies provided strong evidence for strwerries s the vehicle of infection. Conducted in different geogrphicl regions nd using vrious designs, they consistently nd exclusively showed sttisticlly significnt ssocitions etween illness nd the consumption of strwerry dishes. Furthermore, in ll studies, ffected institutions offered strwerry dishes two clendr dys efore the pek of illnesses, nd in one instnce, severl strwerry-contining dishes, served on different dys, cused severl wves of illnesses. Epidemiologicl evidence guided food sfety investigtions on the locl, stte nd ntionl level [12]. Erly identifiction of the vehicle of infection led to timely withdrwl of more thn hlf of the lot. Assuming similr level of contmintion in the prt of the lot tht ws withdrwn, t lest 11, cses were verted y the withdrwl, proly even more, seeing s only frction of the delivered strwerries hd een prepred for consumption. According to the report of the Germn Tsk Force on Food nd Feed Sfety, some of the involved regionl kitchens of Cterer X reported not to hve heted the strwerries during preprtion of the implicted dishes wheres others stted tht they hd, which my in prt explin tht not ll institutions supplied y the involved regionl kitchens reported cses of gstroenteritis [12].In response to this outrek, recommendtions in Germny for institutions ctering for vulnerle popultions (including schools nd child cre fcilities) hve een mended nd now specificlly include the dvice to het frozen erries [13]. Furthermore, from 1 Jnury 213, Europen Union (EU) regultion requires 5% of consignments of frozen strwerries imported from Chin into the EU to e tested for norovirus [14]. Infectious disese outreks due to contminted produce hve gined importnce in the recent pst [15], including norovirus outreks in Europe linked to frozen rsperries [16-22] or lckerries [23] nd the multistte outrek of heptitis A due to mixed frozen erries [24]. Also strwerries hve repetedly een incriminted in lrge heptitis A outreks in the United Sttes [25,26] nd in Europe [27]. Germny hs recently fced numer of outreks cused y contminted vegetles or fruits including sprouts nd wtermelons [28-3]. The originl contmintion of the food vehicles or relevnt ingredients occurred in countries tht were not known to e ffected y outreks, which complicted or even prevented thorough source investigtions. In none of these outreks, including this one, ws the mode of contmintion elucidted. Undoutedly, trnsntionl source investigtions pose prticulr chllenges [31]; politicl nd economic issues my sometimes hmper effective collortion. A etter understnding of how the erries 7

8 ecme contminted is crucil for developing longterm prevention mesures upstrem of the retiler. Severl different norovirus genotypes of genogroups I nd II were detected in the strwerries [8] (nd lso in humn smples) [32]. Together with the lrge scle of the outrek, this lends support to the hypothesis tht the use of contminted wter in the production of the strwerries ws responsile for the outrek. This report exemplifies the risk of lrge outreks in the er of glol food trde. Tody, unprecedented volumes of produce (here 22 tonnes) re distriuted to lrge numer of mrkets throughout the world [33], therey incresing the risk for food sfety. Pulic helth surveillnce needs to dpt to these chllenges, e.g. e le to detect outreks cused y widely disseminted foods. Surveillnce using moleculr sutyping informtion llows estlishing links etween disese occurrences in different regions, usully seemingly spordic cses or smll clusters [34]. The outrek descried here ppered s n ccumultion of concurrent locl outreks in severl djcent sttes. Thus, in ddition to moleculr surveillnce, rpid communiction of locl outreks to the stte level, s it hppened in the outrek-detecting stte of Brndenurg, enles rpid recognition nd investigtion of supr-regionl events even efore the etiology is known, nd should e implemented in routine infectious disese surveillnce. Outrek Investigtion Tem Mon Askr, Brr Gunsenheimer-Brtmeyer, Susnne Behnke, Jnin Breidench, Len Fieig, Andres Gilsdorf, Benedikt Greutélers, Jne Hecht, Juli Hermes, Frnzisk Jentsch, Astrid Milde-Busch, Krin Preußel, Mximilin Prohl, Cornelius Remschmidt, Sine Ritter, Bettin Rosner, Cludi Sntos-Hövener, Lrs Schde, Mdlen Schütze, Kristin Tolksdorf, Mtthis Wetzstein (Roert Koch Institute, Berlin, Germny); Jörg Bätzing-Feigenum (Berlin Stte Office for Helth & Socil Affirs, Berlin, Germny); Hnn Oppermnn (Agency for Consumer Protection of the Federl Stte of Sxony-Anhlt, Mgdeurg, Germny); Anke Popp (Thuringin Stte Authority for Consumer Protection, Bd Lngenslz, Germny). Acknowledgements We thnk the stff of locl nd stte helth deprtments for collecting the dt tht were the sis of the descriptive nlysis. For their support of the nlyticl studies we would like to thnk the prent representtive of school D, the stff of the Locl Helth Deprtment Steglitz-Zehlendorf, nd the Locl Veterinry Authority Chemnitz. Furthermore we would like to cknowledge the help of other collegues in the Deprtment for Infectious Disese Epidemiology nd the Press Deprtment t the RKI during the cute phse of the outrek, nd PAE/EPIET coordintors. Lst ut not lest, we would like to thnk ll study prticipnts, the stff nd the heds of the prticipting schools for their support. No funding ws received for the presented work. Conflict of interest None declred. Authors contriutions HB, MF, HW nd DW drfted the mnuscript. HB nd DW were the principle investigtors of CCS 1, DW of CCS 2, MF of Survey 1, nd SH of Survey 2 (ll sustntilly contriuted to conception nd design, dt collection, nlysis nd interprettion). HB designed the tool used for dt collection nd nlysis in CCS 1 nd 2 nd represented the RKI t the Tsk Force Gstroenteritis collorting with the food sfety uthorities. HW ws responsile for the collection, nlysis nd interprettion of descriptive dt. MH performed the dt nlysis of CCS 1 nd 2. AS sustntilly contriuted to dt interprettion nd represented the RKI t the Tsk Force Gstroenteritis. TD prticipted in dt collection of CCS 1 nd ws principle investigtor of CCS 2 (dt collection nd interprettion). CS ws principle investigtor for the Stte Helth Authority Brndenurg (collection, nlysis nd interprettion of descriptive dt). SSM ws principle investigtor for the Stte Helth Authority Sxony (collection, nlysis nd interprettion of descriptive dt) nd contriuted to the conception of CCS 1. GF coordinted the Germn Tsk Force on Food nd Feed Sfety. OH nd KS sustntilly contriuted to the interprettion of descriptive nd study dt. All uthors criticlly revised the mnuscript nd pproved of the finl version. 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